Developmental Changes in the Metabolic Network of Snapdragon Flowers

Abstract

Evolutionary and reproductive success of angiosperms, the most diverse group of land plants, relies on visual and olfactory cues for pollinator attraction. Previous work has focused on elucidating the developmental regulation of pathways leading to the formation of pollinator-attracting secondary metabolites such as scent compounds and flower pigments. However, to date little is known about how flowers control their entire metabolic network to achieve the highly regulated production of metabolites attracting pollinators. Integrative analysis of transcripts and metabolites in snapdragon sepals and petals over flower development performed in this study revealed a profound developmental remodeling of gene expression and metabolite profiles in petals, but not in sepals. Genes up-regulated during petal development were enriched in functions related to secondary metabolism, fatty acid catabolism, and amino acid transport, whereas down-regulated genes were enriched in processes involved in cell growth, cell wall formation, and fatty acid biosynthesis. The levels of transcripts and metabolites in pathways leading to scent formation were coordinately up-regulated during petal development, implying transcriptional induction of metabolic pathways preceding scent formation. Developmental gene expression patterns in the pathways involved in scent production were different from those of glycolysis and the pentose phosphate pathway, highlighting distinct developmental regulation of secondary metabolism and primary metabolic pathways feeding into it.

Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering

“…The enzymes proficient in using numerous similar substrates, such as acyltransferase and salicylic acid methyltransferase (SAMT), supplied the precursors that controlled the product type (Boatright et al 2004). A relative investigation on the regulation of monoterpenes and benzenoids emission in snapdragon flowers showed that the orchestrated emission of isoprenoids and phenylpropanoid compounds were regulated upstream by individual metabolic pathways (Muhlemann et al 2012).…”

Floral Metabolism of Sugars and Amino Acids: Implications for Pollinators’ Preferences and Seed and Fruit Set

“…Indeed, a biochemical reprogramming occurring at (or around) anthesis has been documented in numerous plant species. For example, in petals of Antirrhinum majus (snapdragon), chlorophyll content decreases at anthesis (Muhlemann et al, 2012), and similarly, in Arabidopsis, the dismantling of the photosynthetic apparatus, which follows the conversion of chloroplasts to chromoplasts, starts soon after the flowers open (Wagstaff et al, 2009). This shift from autotrophic to heterotrophic metabolism is transcriptionally regulated and marks the moment when flower secondary metabolism becomes predominant (Muhlemann et al, 2012;Tsanakas et al, 2014).…”

“…For example, in petals of Antirrhinum majus (snapdragon), chlorophyll content decreases at anthesis (Muhlemann et al, 2012), and similarly, in Arabidopsis, the dismantling of the photosynthetic apparatus, which follows the conversion of chloroplasts to chromoplasts, starts soon after the flowers open (Wagstaff et al, 2009). This shift from autotrophic to heterotrophic metabolism is transcriptionally regulated and marks the moment when flower secondary metabolism becomes predominant (Muhlemann et al, 2012;Tsanakas et al, 2014). As glycolysis and the pentose phosphate pathway are transcriptionally down-regulated and floral secondary metabolic pathways are up-regulated, the concentrations of metabolic intermediates of the tricarboxylic acid cycle, such as fumarate and malate, also decline, while the content of volatile organic compound precursors, such as the aromatic amino acids Phe and Tyr, increases progressively (Muhlemann et al, 2012).…”

“…This shift from autotrophic to heterotrophic metabolism is transcriptionally regulated and marks the moment when flower secondary metabolism becomes predominant (Muhlemann et al, 2012;Tsanakas et al, 2014). As glycolysis and the pentose phosphate pathway are transcriptionally down-regulated and floral secondary metabolic pathways are up-regulated, the concentrations of metabolic intermediates of the tricarboxylic acid cycle, such as fumarate and malate, also decline, while the content of volatile organic compound precursors, such as the aromatic amino acids Phe and Tyr, increases progressively (Muhlemann et al, 2012). Indeed, the physiological function of petals is to attract animal pollinators to flowers, for which pigments and scented molecules are synthesized.…”

Reflectance of botanical, production and geographical origin on the unique compositional traits of purple grape juices

“…In addition, intraregional differences between the production systems were observed (juices produced classes. Differences in the profile and ion intensities are probably related to the various biosynthesis pathways regulators (enzyme protein content and the expression of corresponding structural genes) in response to biotic interactions (pathogens and herbivores) and multiple environmental and technological factors used to produce the grapes and the juice, respectively, such as light intensity, atmospheric CO2 concentration, soil type and chemical composition, temperature, relative humidity, and nutrient status (Muhlemann et al, 2012;Dudareva, Klempien, Muhlemann, & Kaplan, 2013). It is also hypothesized that the level and type of nitrogen and phosphorus may also be responsible for the content of VOCs in grape juice.…”